Genetic and genomic analyses reveal boundaries between species closely related to <i>Cryptococcus</i> pathogens

Passer, Andrew Ryan; Coelho, Marco A.; Billmyre, R. Blake; Nowrousian, Minou; Mittelbach, Moritz; Yurkov, Andrey; Averette, Anna Floyd; Cuomo, Christina A.; Sun, Sheng; Heitman, Joseph

doi:10.1101/557140

Cited by 8 publications

(21 citation statements)

References 106 publications

(129 reference statements)

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“…An instance of physically linked MAT loci has been well-studied in Cryptococcus neoformans, a member of a group of closely related, pathogenic Cryptococcus species [1]. Fusion of the HD and P/R loci most likely occurred in the ancestor of the pathogenic Cryptococci, because other analyzed Tremellales species including the closely related, but non-pathogenic Cryptococcus amylolentus, Kwoniella heveanensis, Kwoniella mangrovensis, Cryptococcus wingfieldii, and Cryptococcus floricola are all tetrapolar [33][34][35][36][37]. The C. neoformans MAT locus, which consists of genetically linked HD and P/R loci, encompasses more than 20 genes over a region spanning more than 100 kb and has two alleles designated a and α.…”

Section: Introductionmentioning

confidence: 99%

Convergent evolution of linked mating-type loci in basidiomycete fungi

et al. 2019

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Sexual development is a key evolutionary innovation of eukaryotes. In many species, mating involves interaction between compatible mating partners that can undergo cell and nuclear fusion and subsequent steps of development including meiosis. Mating compatibility in fungi is governed by the mating type (MAT) loci. In basidiomycetes, the ancestral state is hypothesized to be tetrapolar, with two genetically unlinked MAT loci containing homeodomain transcription factor genes (HD locus) and pheromone and pheromone receptor genes (P/R locus), respectively. Alleles at both loci must differ between mating partners for completion of sexual development. However, there are also basidiomycetes with bipolar mating systems, which can arise through genomic linkage of the HD and P/R loci. In the order Tremellales, bipolarity is found only in the pathogenic Cryptococcus species. Here, we describe the analysis of MAT loci from 24 species of the Trichosporonales, a sister order to the Tremellales. In all of the species analyzed, the MAT loci are fused and a single HD gene is present in each mating type, similar to the organization in the pathogenic Cryptococci. However, the HD and P/R allele combinations in the Trichosporonales are different from those in the pathogenic Cryptococci. This and the existence of tetrapolar species in the Tremellales suggest that fusion of the HD and P/R loci occurred independently in the Trichosporonales and pathogenic Cryptococci, supporting the hypothesis of convergent evolution towards fused MAT regions, similar to previous findings in other fungal groups. Unlike the fused MAT loci in several other basidiomycete lineages though, the gene content and gene order within the fused MAT loci are highly conserved in the Trichosporonales, and there is no apparent suppression of recombination extending from the MAT loci to adjacent chromosomal regions, suggesting different mechanisms for the evolution of physically linked MAT loci in these groups.

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Section: Introductionmentioning

confidence: 99%

Convergent evolution of linked mating-type loci in basidiomycete fungi

et al. 2019

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“…Compared to other basidiomycetes, the C. neoformans MAT locus is unusually large, spanning more than 100 kb and containing more than 20 genes. Studies have shown that the MAT locus in C. neoformans is a fusion product of the ancestral P/R and HD loci, and thus includes genes encoding both homeodomain transcription factors (HD), as well as pheromones and pheromone receptors (P/R) (LOFTUS et al 2005;HSUEH et al 2011;SUN et al 2017;PASSER et al 2019).…”

Section: Introductionmentioning

confidence: 99%

“…Cryptococcus amylolentus, together with Cryptococcus floricola and Cryptococcus wingfieldii, are the most closely related known sibling species of the C. neoformans/C. gattii pathogenic species complex (FINDLEY et al 2009;PASSER et al 2019). C. amylolentus has a tetrapolar mating system with the two mating type loci (A and B) located on different chromosomes.…”

Section: Introductionmentioning

confidence: 99%

The pheromone and pheromone receptor mating-type locus is involved in controlling uniparental mitochondrial inheritance inCryptococcus

Sun

Ianiri

et al. 2019

Preprint

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Mitochondria are inherited uniparentally during sexual reproduction in the majority of eukaryotic species studied, including humans, mice, nematodes, as well as many fungal species. Mitochondrial uniparental inheritance (mito-UPI) could be beneficial in that it avoids possible genetic conflicts between organelles with different genetic backgrounds, as recently shown in mice; and it could prevent the spread of selfish genetic elements in the mitochondrial genome. Despite the prevalence of observed mito-UPI, the underlying mechanisms and the genes involved in controlling this non-mendelian inheritance are poorly understood in many species. In Cryptococcus neoformans, a human pathogenic basidiomyceteous fungus, mating types (MATα and MATa) are defined by alternate alleles at the single MAT locus that evolved from fusion of the two MAT loci (P/R encoding pheromones and pheromone receptors, HD encoding homeodomain transcription factors) that are the ancestral state in the basidiomycota. Mitochondria are inherited uniparentally from the MATa parent in C. neoformans and this requires the SXI1α and SXI2a HD factors encoded by MAT. However, there is evidence additional genes contribute to control of mito-UPI in Cryptococcus. Here we show that in Cryptococcus amylolentus, a sibling species of C. neoformans with unlinked P/R and HD MAT loci, mitochondrial uniparental inheritance is controlled by the P/R locus, and is independent of the HD locus.Consistently, by replacing the MATα alleles of the pheromones (MF) and pheromone receptor (STE3) with the MATa alleles, we show that these P/R locus defining genes indeed affect mito-UPI in C. neoformans during sexual reproduction. Additionally, we show that during early stages of C. neoformans sexual reproduction, conjugation tubes are always produced by the MATα cells, resulting in unidirectional migration of the MATα nucleus into the MATa cell during zygote formation. This process is controlled by the P/R locus and could serve to physically restrict movement of MATα mitochondria in the zygotes, and thereby contribute to mito-UPI. We propose a model in which both physical and genetic mechanisms function in concert to prevent the coexistence of mitochondria from the two parents in the zygote and subsequently in the meiotic progeny, thus ensuring mito-UPI in pathogenic Cryptococcus, as well as in closely related non-pathogenic species.The implications of these findings are discussed in the context of the evolution of mito-UPI in fungi and other more diverse eukaryotes.

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“…It is homothallic, self‐fertile fungal species with a continuously activated sexual cycle 18 . Divergence of pathogenic species from their non‐pathogenic ancestors is largely attributed to chromosomal alterations in the MAT loci, which are also the probable cause of the change from the tetrapolar sexual cycle in C. amylolentus and C. wingfieldii to the bipolar sexual cycle in pathogens 13,14,16,18 …”

Section: Sexual Reproductionmentioning

confidence: 99%

Diverse species in the genus Cryptococcus: Pathogens and their non‐pathogenic ancestors

2020

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The genus Cryptococcus comprises of more than 30 species. It consists of clinically significant pathogenic Cryptococcus neoformans/Cryptococcus gattii species complex comprising of a minimum of seven species. These pathogens cost more than 200,000 lives annually by causing cryptococcal meningoencephalitis. The evolution of the pathogenic species from closely related nonpathogenic species of the Cryptococcus amylolentus complex is of particular importance and several advances have been made to understand their phylogenetic and genomic relationships. The current review briefly describes the sexual reproduction process followed by an individual description of the members focusing on their key attributes and virulence mechanisms of the pathogenic species. A special section on phylogenetic studies is aimed at understanding the evolutionary divergence of pathogens from non-pathogens. Recent findings from our group pertaining to parameters affecting codon usage bias in six pathogenic and three non-pathogenic ancestral species and their corroboration with existing phylogenetic reports are also included in the current review.

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Genetic and genomic analyses reveal boundaries between species closely related to Cryptococcus pathogens

Cited by 8 publications

References 106 publications

Convergent evolution of linked mating-type loci in basidiomycete fungi

Convergent evolution of linked mating-type loci in basidiomycete fungi

The pheromone and pheromone receptor mating-type locus is involved in controlling uniparental mitochondrial inheritance inCryptococcus

Diverse species in the genus Cryptococcus: Pathogens and their non‐pathogenic ancestors

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